Significance of Perylene for Source Allocation of Terrigenous Organic Matter in Aquatic Sediments

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Cite This: Environ. Sci. Technol. 2019, 53, 8244−8251 pubs.acs.org/est

Signiﬁcance of Perylene for Source Allocation of Terrigenous Organic Matter in Aquatic Sediments † † ∥ † ‡ § † Ulrich M. Hanke,*, Ana L. Lima-Braun, , Timothy I. Eglinton, , Jeﬀrey P. Donnelly, Valier Galy, † ⊥ † § § † Pascale Poussart, , Konrad Hughen, Ann P. McNichol, Li Xu, and Christopher M. Reddy † Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, Massachusetts 02543, United States ‡ Geological Institute, ETH Zürich, Sonneggstrasse 5, 8092 Zurich, Switzerland § Department of Geology and Geophysics, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, Massachusetts 02543, United States

*S Supporting Information

ABSTRACT: Perylene is a frequently abundant, and some- times the only polycyclic aromatic hydrocarbon (PAH) in aquatic sediments, but its origin has been subject of a longstanding debate in geochemical research and pollutant forensics because its historical record differs markedly from typical anthropogenic PAHs. Here we investigate whether perylene serves as a source-specific molecular marker of fungal activity in forest soils. We use a well-characterized sedimentary record (1735−1999) from the anoxic-bottom waters of the Pettaquamscutt River basin, RI to examine mass accumulation rates and isotope records of perylene, and compare them with total organic carbon and the anthropogenic PAH fluoranthene. We support our arguments with radiocarbon (14C) data of higher plant leaf-wax n-alkanoic acids. Isotope-mass balance-calculations of perylene and n-alkanoic acids indicate that ∼40% of sedimentary organic matter is of terrestrial origin. Further, both terrestrial markers are pre-aged on millennial time-scales prior to burial in sediments and are insensitive to elevated 14C concentrations following nuclear weapons testing in the mid-20th Century. Instead, changes coincide with enhanced erosional flux during urban sprawl. These findings suggest that perylene is definitely a product of soil-derived fungi, and a powerful chemical tracer to study the spatial and temporal connectivity between terrestrial and aquatic environments.

■ INTRODUCTION determined that the fungal species Cenococcum geophillum Downloaded via MBLWHOI LIBRARY on December 1, 2020 at 16:47:21 (UTC). 1−5 6−8 produces 4,9-dihydroxyperylene-3,10-quinone, confirming a Perylene is found in marine and lacustrine sediments, 1,22 soils,9,10 and also petroleum11,12 and fuel emissions13,14 often longstanding hypothesis that there is a naturally produced precursor. This ectomycorrhizal fungus appears almost ubiq- See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. associated with other distinctive anthropogenic combustion- derived polycyclic aromatic hydrocarbons (PAHs). However, uitous in boreal, temperate, and subtropical regions, and most studies report that sediment records of perylene differ is present in the rhizosphere of woody-plant roots and more − 26 greatly from those of anthropogenic PAHs.15 19 The latter are generally in forest soils. A fungal origin can explain the typically most abundant in sediments post-dating the Industrial widespread abundance of perylene in the environment even over 27 Revolution, particularly those deposited during the latter half of geological time-scales, since mycorrhizal associations with 28 the 20th Century, whereas perylene abundances are lowest near vascular plants evolved about 400 million years ago. the sediment−water interface and tend to increase with depth, Besides C. geophyllum, other mycorrhiza also produce similar 29,30 particularly in anoxic sedimentary settings.18,20 This depth- perylene precursor compounds as toxins involved in 31 related increase in concentration implies abiotic or biologically pathogenesis of their host plant. Prior stable carbon isotopic mediated in situ production from precursor natural prod- (δ13C) measurements of perylene found values similar to those 2,21 δ13 ≈− ‰ uct(s) by either a first- or second-order reaction under of terrestrial sources (C3-vegetation: C 27 ), anaerobic conditions.20 The origin of perylene has remained unclear for decades, Received: April 17, 2019 1,2,22,23 during which has previously been argued for terrestrial Revised: June 11, 2019 and diagenetic,6,16,24 as well as petrogenic12,25 and pyrogen- Accepted: June 19, 2019 ic13,14 sources. It was only recently that Itoh and collaborators23 Published: June 19, 2019

© 2019 American Chemical Society 8244 DOI: 10.1021/acs.est.9b02344 Environ. Sci. Technol. 2019, 53, 8244−8251 Environmental Science & Technology Article supporting a wood-degrading origin from the rhizosphere.32 (41.503100; −71.450500) in 1999. The catchment area covers This is further supported by dual-isotope analyses of perylene 35 km2 of forest, wetlands and open water of which today about (δ13C and δD) in sediments showing similar δD values as 30% is residential land.37 Ocean water flooded the basin about methoxy groups in lignin while δ13C values are consistent with 1700 ± 300 years ago leading to a stratified water column and the expected fractionation range in saprophytic fungi.22 In sustained anoxic conditions in bottom waters and underlying addition, natural abundance radiocarbon (14C) analyses allows a sediments.36 A detailed description on the sediment chronology comparison of the 14C age of perylene with that of other organic and sample processing is presented elsewhere.15,39 Sediment matter constituents,25 including total organic carbon (TOC) chronology was obtained fromvarvecountingofX-ray and specific markers of terrigenous organic matter co-deposited radiographs as well as from 137Cs and 210Pb profiles using the in aquatic sediments. Such analyses shed light on the origin and model of constant rate of supply that yielded a sequence of about provide further evidence on the origin of perylene and its use in 260 years (1735−1999 AD) and an average sedimentation rate environmental forensics. of 0.44 ± 0.10 cm yr−1.39 Our motivation is to reconcile existing hypotheses on the Sections from the cores were combined after aligning x- source of perylene and assess the potential of this marker radiograph images including hurricane layers in 1938 and 1954 compound as a biogeochemical tracer to follow the trajectories to a reference chronology of varve counting, 210Pb, and 137Cs. of terrigenous organic matter mobilization and transport within This was necessary to obtain enough sediment for trace fi 35 watersheds. Speci cally, we investigate whether it serves as a molecular isotopic-analyses. Hence, we pooled the samples molecular marker for rhizosphere carbon from catchment soils in eight horizons for all isotopic analyses: H1 (1999−1982), H2 and thus facilitates source approximation of terrigenous organic (1981−1962), H3 (1960−1931), H4 (1929−1898), and H5 matter in sediments. Moreover, while researchers currently tend (1896−1873), H6 (1871−1842), H7 (1840−1768), and H8 to exclude perylene from forensic investigations involving the (1764−1735), respectively, except n-alkanoic acids that were apportionment of PAHs due to its incongruent behavior, analyzed in four individual samples: 1885 ± 5, 1947 ± 33, 1972 ff 33,34 perylene may have mutagenic e ects on organisms. Thus, an ± 2, and 1991 ± 1. Quantitative measurements for the improved understanding of the provenance and dynamics of calculation of the mass accumulation rates as well as grain size perylene may be pertinent to mapping inventories of natural and analyses were performed on individual samples as well. anthropogenic pollutants, delineating transport pathways, and Grain Size Analyses. One freeze-core slab was subsectioned reconstructing historical land-use. using a scalpel blade, transferred into 50 mL round-bottom In this study, we construct historical records of perylene and flasks and treated with a 30% hydrogen peroxide solution at a TOC abundances and isotope compositions from the anoxic ratio of 40 mL per 1 g sediment, and heated in a water bath to 70 sediments of the suburban Pettaquamscutt River basin, RI. We °C as a means to support mineralization of the organic matter. chose these sediments because they provide an exceptionally Subsequently, samples were freeze-dried, and a subsample of detailed chronological record and a wealth of background about 11 mg was suspended in water and measured on a information on the catchment area, including human influence − Beckmann Coulter LS13 320 laser diffraction particle analyzer on local to regional scales.15,35 38 In addition, this sedimentary (Indianapolis, IN) in triplicate. record extends over 260 years, from the preindustrial (∼1735) Total Organic Carbon and Nitrogen. A Fisons 1108 until 1999, including an interval characterized by frequent elemental analyzer was used to measure the TOC content of the above-ground nuclear-bomb testing (resulting in elevated samples. To remove the inorganic carbon fraction, about 2 mg of atmospheric 14C concentrations peaking in 1963 when the dry sample was weighed into a silver capsule and acidified with testing ceased), thus offering the opportunity to study the rate at 20 μL of 2 N HCl. TOC content was calculated in relation to the which specific organic carbon species incorporate atmospheric whole sediment dry weight while organic carbon/organic CO2 and are sequestered in aquatic sediments. These character- istics of the study site, when coupled with down-core δ13C and nitrogen TOC/TN ratios were calculated on an atomic basis. 14C records, provide a novel perspective on perylene Samples were run in triplicate and all reported weight percentages represent the mean ± one standard deviation with biogeochemistry, yielding constraints on its source and on the an instrumental blank of 0.004 mg for C and smaller than 0.005 burial efficiency of terrigenous organic matter in aquatic mg for N. sediments. We compare mass accumulation rates (MAR) of Isotope Ratio Monitoring Mass Spectrometry. The perylene and TOC to the combustion-derived PAH marker stable carbon isotopic composition of bulk sample TOC was fluoranthene. While several nonalkylated PAHs could be used to trace past-combustion practices, we choose fluoranthene determined in triplicate by automated online solid combustion because its quantitative down-core profile resembles the interfaced to a Finnigan Delta Plus isotope ratio mass temporal evolution of the sum of 15 parent PAHs in this spectrometer. Isotope ratios were calculated relative to CO2 watershed.15 We further support our interpretation with down- reference gas pulses, with standard deviations for replicate measurements were always better than 0.6‰ and usually within core data of particle size and leaf wax (C30−32; n-alkanoic acids) ‰ 14C variations. We then carefully assess whether the rhizosphere 0.3 . Extraction, Purification, and Isotope Analyses of of wooded land serves as the direct source for perylene in the Perylene, Fluoranthene, and n-Alkanoic Acids. environment and discuss the process of pre-aging of terrestrial Dry sediment samples (0.5−1.5 g) were extracted by pressurized organic matter prior to delivery into the aquatic environment in fl the context of parallel sedimentary records. uid extraction (Dionex ASE 200) using a mixture of acetone and n-hexane (1:1) at 1000 psi at 100 °C. Molecular identification and quantification was achieved using an Agilent ■ EXPERIMENTAL SECTION 6890 Plus GC System interfaced to a mass selective detector A series of seven freeze cores were collected in the depocenter of operating at 70 eV in SIM mode using a DB-XLB capillary the lower basin of the Pettaquamscutt River basin, RI column (60 m × 0.25 mm × 0.25 μm).15

8245 DOI: 10.1021/acs.est.9b02344 Environ. Sci. Technol. 2019, 53, 8244−8251 Environmental Science & Technology Article

Figure 1. Mass accumulation rates for total organic carbon (TOC), perylene, and fluoranthene as well as carbon to nitrogen (TOC/TN) ratios and fl fi down-core shifts in coarse particle abundance (D90) with shaded area A representing the maximum PAH ux in this area, B the period of ampli ed erosion due to infrastructure development, and C the preindustrial era prior to 1840s.

Compound-specific radiocarbon analyses (CSRA) of per- chromatograph.41 Following the chromatographic purification ylene and fluoranthene were performed on eight pooled of individual compounds, samples were graphitized and horizons by first using high-pressure liquid-chromatography measured at NOSAMS, Woods Hole, MA. (HPLC) to separate pure perylene (98% purity or greater) from Evaluation of Isotope Data. Isotope mass-balance the sample extracts. The HPLC procedure isolated PAHs into 2- calculations provide quantitative estimates for source apportion- ring and the combined 3 + 4-ring and 5 + 6-ring PAHs. The ment of organic matter. To constrain the sources of TOC and resulting 16 HPLC fractions (8 horizons × 2 ring classes) were perylene in Pettaquamscutt River sediments, we calculated the subjected to two-dimensional preparative capillary gas chroma- relative contribution of possible organic carbon sources in the fi tography for isolation and puri cation of individual PAHs via sediments using the measured 14C and δ13C values for TOC HP 7683 autoinjector and a multicolumn switching system (Figure 2). We report the 14C data as F14C which is the fraction (Gerstel MCS 2) connected to a HP 6890 series gas modern independent from the year of measurement.42 We chromatograph, and Gerstel preparative fraction collector assumed a simple mixing model to retrieve an average value for (PFC; further details in the Supporting Information (SI)). the time lag of perylene and leaf wax n-alkanoic acids; the details Purified samples were transferred to precombusted quartz tubes 35 × of which are published elsewhere. In brief, these source- (7 mm i.d. 20 cm), dried under nitrogen before adding copper specific molecular markers facilitate approximations of the oxide (50 mg). Each tube was then evacuated on a vacuum line contributions of terrigenous organic matter in aquatic sediments while samples were kept at −90 °C to prevent sublimation, (further details on the concept are included in the SI). sealed, and combusted at 850 °C for 5 h. About 95% of the To account for the potential variability under increasing purified carbon dioxide was reduced to graphite, pressed and human pressure on the coastal environment, we determined analyzed for 14C at NOSAMS, Woods Hole, MA, and the δ13 average values of our terrestrial end-members for two time remaining 5% was used for C measurements. − “ ” δ13 periods: the preindustrial (1735 1840) and the post- bomb The C values of perylene were also determined in triplicate − 14 on a Finnigan Delta Plus isotope ratio mass spectrometer with (1960 1999) period (see SI for more detail). Regarding C attached Finnigan GC combustion III interface and Hewlett- data evaluation, the post-1960s period also is a benchmark to Packard 6890 GC (irm-GC/MS). Compounds were separated test for the resilience and short-term dynamics of catchment ff on a CP-Sil 5CB capillary column (50 m × 0.25 mm × 0.25 μm) processes. In contrast, the aquatic end-member is only a ected ff ± 14 and isotope ratios for PAH peaks were calculated relative to CO by the marine reservoir e ect, which is about 400 40 C years 2 14 reference gas pulses. The standard deviation for replicate lower than the atmospheric C concentration at the time of 43 measurements of perylene was better than 0.6 ‰ and mostly burial. Furthermore, we neglect a potential impact of 44 around 0.2 ‰. petrogenic carbon in the Pettaquamscutt River because of The isotopic composition of leaf wax n-alkanoic acids the absence of postglacial erosion and due to the absence of 45 (C30−32) were determined for four individual sediment samples carbonaceous metasedimentary rocks in the basin. We deposited in 1885 ± 5, 1947 ± 33, 1972 ± 2, and 1991 ± 1 constrain our model by δ13C=−21.0‰ for aquatic following the analytical procedure described elsewhere.40 In production46 and use local records of perylene, pyrogenic fi 35 fi brief, n-alkanoic acids were extracted, isolated, and puri ed using carbon and n-alkanoic acids (C30−32)tode ne terrestrial end- a preparative Hewlett-Packard 5890 series II capillary gas members. We further obtained the contemporary atmospheric

8246 DOI: 10.1021/acs.est.9b02344 Environ. Sci. Technol. 2019, 53, 8244−8251 Environmental Science & Technology Article

Figure 2. High-resolution δ13C record for TOC and pooled sample results for perylene (left); molecular 14C data for the combustion-derived ﬂuoranthene (middle) and results on perylene, leaf wax n-alkanoic acids as well as TOC (right).

14C concentrations from the extended Intcal13 reference composed of labile material with C/N values similar to aquatic chronology.43,47 organic matter (C/N = 4 to 10).48 However, we refrain from further speculations on this bulk-level information due to the ■ RESULTS AND DISCUSSION absence of a robust reference for C/N values of terrigenous The exceptionally well-constrained chronology of the Petta- organic matter from this area. MARs for perylene (and proto-perylene), which corresponds quamscutt River sediments along with detailed reconstructions μ −2 of the provenance of combustion-derived PAHs15,35 and Hg38 to the reduced perylenequinone, vary from 29 to 3800 gm yr−1, while its down-core profile differs markedly from the provide key constraints that allow us to determine whether fl perylene signatures are consistent with its production in the combustion-marker uoranthene (Figure 1). The values were rhizosphere of catchment soils.23,26 To characterize the export of low before 1938, reached a maximum between ca. 1938 and μ −2 −1 terrigenous organic matter, including the putative precursors of 1973 (1580 gm yr ), before diminishing again in most recent decades (∼ 100 μgm−2 yr−1)(Figure 1). This contrasting perylene, and its subsequent burial in aquatic sediments, we ff report MAR for TOC, perylene, and fluoranthene. Isotopic mass accumulation behavior implies a di erent origin for perylene δ13 14 relative to combustion-derived PAHs, here illustrated by balance calculations for C and C records are employed to fl further constrain the main source of perylene precursors. With uoranthene (Figure 1). This nonalkylated PAH appears μ −2 −1 reference to recent research and our results, we then provide a lower in abundance varying from 1 to 1280 gm yr and fi 35 synthesis aiming to merge the existing concepts, reconciling the also exhibits signi cant variability, however the temporal ff origin of perylene (i.e., terrestrial, diagenetic or petro-/ evolution of MARs of this pyrogenic PAH di ers sharply from fi fl ’ pyrogenic). that of perylene. Speci cally, uoranthene s MAR was low until Down-Core Mass Accumulation Rates of TOC and the mid-19th century (Figure 1C), increased steadily to a Perylene. The burial rate of TOC in the sediments of the maximum in the late-1950s, then declined in the post-1970s due Pettaquamscutt River ranges from 38 to 61 g m−2 yr−1 (average to cleaner burning fuels and as consequence of environmental 15,37 =49± 6gm−2 yr−1, n = 71). The lowest TOC burial flux is regulations. Such down-core profiles of combustion-derived observed in ca. 1938 (Figure 1) and is related to a 16.7% shift in PAHs are also observed in other sedimentary records, including 16,19,49 burial flux from 53.0 ± 43 g m−2 yr−1 prior to ca. 1927 to 44.0 ± the upper basin of the Pettaquamscutt River. 3.7 g m−2 yr−1 for sediments deposited thereafter. The timing of The observed decline in perylene (and proto-perylene) MAR this change coincides with the construction of the Lacey Bridge between 1927 and 1938 coincides with the abrupt decrease in on the ocean side of the lower basin in 193445 (Figure 1B) that TOC accumulation rate (Figure 1B). We attribute the latter to a likely caused a restriction in seawater intrusion, affecting the dilution in organic carbon content resulting from a higher influx of both marine as well as the terrestrial matter. We argue proportion of clastic material due to erosion of soil mineral that this exemplifies the accelerated development of the horizons (Figure 1). Perylene is a trace constituent of TOC, catchment area beginning early in the last century and the never accounting for more than 0.1% of TOC, and consequently related infrastructure projects that changed the natural flow perylene/TOC ratios shift by 500% relative to before or after paths of materials within the watershed. this time interval. These observations thus support the link ’ The Norg down-core record reveals only small variations, here between a decrease in perylene s MAR resulting from an increase fi fl illustrated as Corg/Norg pro les (n = 71; Figure 1) where three in erosional ux (Figure 1B). trends are delineated: decreasing C/N from 1730s (12.6) to A striking feature of the perylene profile is that fluxes remain − − 1840s (9.4), a ∼50-year reversal toward higher C/N ratios (13.2 nearly constant (665 ± 180 μgm 2 yr 1; n = 26) prior to 1865, in 1900), and a century-long C/N secular decrease in the upper indicating either steady-state erosional conditions or quantita- core (10.0 in 1999). This rather narrow range in C/N ratios tive conversion of precursor material (Figure 1).23 Due to the suggests that organic matter is predominantly yet not exclusively large variations in perylene burial rates in our sedimentary

8247 DOI: 10.1021/acs.est.9b02344 Environ. Sci. Technol. 2019, 53, 8244−8251 Environmental Science & Technology Article record we refrain from attempting to derive kinetic parameters data provide additional information on the time scales of organic for conversion of perylenequinone (proto-perylene) precursor matter storage and transport from its source to the “ultimate” to perylene. However, Slater and collaborators50 compared two site of burial. This “residence time” has been determined for − perylene profiles from Lake Siskiwit collected in 1983 and 2005. several markers of terrestrial primary productivity,54 56 as well They found a reaction rate constant (0.048 yr−1), ca. 75% higher as charred plant biomass,35,57 and range from centuries to several than previously reported,20 whereas another study reported millennia. The underlying processes resulting in organic matter much lower rates.18 All of the above studies suggest that the “pre-aging” prior to burial in aquatic depocenters can complicate conversion of perylenequinone to perylene follows first-order source apportionment because the 14C concentration of various kinetics. Nevertheless, the strong (∼ 97%) decrease in perylene organic matter components differs from that of the correspond- abundance in Pettaquamscutt River sediments from 1973 to ing atmospheric 14C reference value. 1999 likely reflects incomplete conversion of precursor We determined an average 14C residence time for perylene of compounds (Figure 1). 1300 ± 300 14C years for samples pre-dating the industrializa- Isotope Mass Balance Calculations. The δ13C TOC tion (1735−1840, n = 3) and 2000 ± 500 14C years for the post- profile (Figure 2) appears relatively invariant throughout the “bomb” era (1960−1999; n = 3). These values agree well with − − ‰ − ± ‰ ± 14 core ( 25.4 to 23.0 , average 24.1 0.5 , n = 36), leaf wax n-alkanoic acids (C30−32) that showed a 2700 700 C indicating the absence of large variations in organic matter year residence time for the post-“bomb” era (Figure 2), and a composition. Although the TOC MAR decreased in the 1930s, record of biomass-derived pyrogenic carbon from the same core δ13C values do not suggest this was accompanied by a shift in the revealed an average age of 1460 ± 490 14C years for the nature of organic matter supplied to Pettaquamscutt River basin. preindustrial era.35 The apparent average age or residence time Instead, the observed changes in burial flux in this catchment are over the preindustrial and the post-“bomb” era for perylene and attributed to a shift in land use stemming from an increase in the higher plant n-alkanoic acids of ca. 2000 14C years is slightly local human population and the accompanied development of higher than it has been reported for (micro) charcoal in the same infrastructure. The δ13C values of perylene (−28.9 to −28.3‰; catchment35 as well as for leaf wax n-alkanoic acids in the Bengal average −28.6 ± 0.6‰; Figure 2) were similarly invariant, while fan55 yet similar to that of Cariaco basin.56 However, in the significantly lower than TOC and similar to that reported for post“bomb” era we observed a decoupling of 14C concentrations − − − ‰ 51 fi terrestrial C3 plants ( 29 to 25, average 28 ). among molecular markers and TOC. Speci cally, the increase in In contrast, the 14C record of TOC for pooled samples (n =8; atmospheric 14C concentrations post-1960s is not apparent in Figure 2) reveals only small variations in preindustrial time perylene or n-alkanoic acids, suggesting that soil carbon storage (1735−1840) but then tends to shift toward more 14C depleted on millennial time scales may conceal or delay the legacy. values between 1839 and 1958. This change is thought to Isotope mass balance calculations based on TOC 13C and 14C integrate the increasing use of fossil fuels slightly diluting the data yield similar values for the proportion of organic matter of natural atmospheric 14C concentration (the so-called “Suess terrestrial origin (δ13C: −43 ± 10% and 14C: −37 ± 10%), with effect”) as well as ongoing infrastructural development and the remaining carbon derived from aquatic productivity. These constructions within the catchment resulting in the mobilization results for the Pettaquamscutt River basin are slightly higher of deeper mineral soils. Thereafter, we observed a drastic than an estimated global average of one-third of sedimentary (∼15%) increase in F14C TOC values reflecting the shift in organic is of terrestrial origin.58 The similar estimates obtained atmospheric 14C derived from thermonuclear weapons testing in from dual-carbon isotope evaluations based on perylene the post-1960s. The uppermost sediment layer signals declining reinforce its value in constraining the terrestrial end-member 14C concentrations similar to the atmosphere.47 in source apportionment. Compound-specific radiocarbon analysis reveals that the 14C New Constraints on the Source of Perylene. The origin profile of perylene follows that of TOC from the preindustrial and widespread distribution of perylene in the environment has period until ∼1950. Thereafter, 14C of TOC increases due to the been a subject of scientific debate for decades, although its incorporation of atmospheric bomb 14C, while perylene tends to conversion from the precursor molecule, 4,9-dihydroxyper- more 14C-depleted values. This could reflect a pyrogenic (fossil ylene-3,10-quinone, has long been suspected.1,2,23,29 In fuel) contribution to perylene, mitigating the impact of “bomb” particular, it has remained unclear whether perylene is formed carbon in the Pettaquamscutt River sediments. However, CSRA during in situ diagenesis6,16 or is of petro-/pyrogenic 11,14,25,59 of leaf wax n-alkanoic acids (C30−32) from the same sediments origin. The former hypothesis was stimulated by the reveals a concomitant 14C trend with perylene (Figure 2). We presence of perylene in Antarctic marine sediments60 and by infer, therefore, that leaf waxes and perylene share a common large similarities between perylene and total organic matter source and mode of export, implying that local erosional fluxes down-core profiles, fueling the notion of in situ synthesis from and mobilization of soil organic matter are responsible for the TOC.16 Along these lines, Gschwend and collaborators20 decoupled TOC and perylene post-1950s signals rather than calculated kinetic parameters necessary to yield perylene from global-scale perturbations such as “Suess effect” or above- biogenic precursor concentrations that are consistent with ground nuclear weapons testing. results from a recent study comparing down-core profiles 20 In the mainly wooded catchment area of Pettaquamscutt years apart in Lake Siskiwit,50 and both are in line with the River, organic molecules are produced during photosynthetic observed reduction of perylenequinones.23 The second activity, translocated and metabolized in plants, as well as alternative hypothesis is based on the abundance of perylene released into the rhizosphere. In soil, plants and animals, in ancient sediments,22,61 fossil fuels11,12 or combustion residues can be assimilated, stabilized and metabolized until they emissions.13,14,59 Regarding the latter sources, perylene eventually become respired to carbon dioxide,52 or they can be concentrations remain below 1.4% of the total PAH and thus eroded and redistributed within the watershed.53 Source-specific are negligible for the overall budget. Its presence in these molecular markers allow delineation of specific processes matrices, however, raises the question of whether perylene is associated with organic matter cycling, while molecular 14C exclusively of fungal origin. A possible explanation for the

8248 DOI: 10.1021/acs.est.9b02344 Environ. Sci. Technol. 2019, 53, 8244−8251 Environmental Science & Technology Article occurrence of perylene in fossil fuels lies in the evolutionary Similarities between TOC and perylene records have been development of fungi. The symbiotic interaction between fungi observed previously,6,16,22,61 yet in these cases it was suspected and vascular plants evolved about 400 Ma ago, and to reflect direct in situ microbial production of perylene16 rather ectomycorrhiza have existed for at least 56 Ma,62 while the than the reduction and conversion of a precursor into perylene. divergence and evolution of the mycorrhiza gene pool remains This depletion of the precursor pool may continue over largely unexplored.28 However, Blumer proposed the con- geological time scales,63 thus limiting comprehensive quantita- 50 version of pigments to hydrocarbons through a geochemically tive assessment of perylene in recent sediments. In contrast, irreversible deoxygenation of functional groups and hydro- the isotopic composition of perylene is expected to be genation under sustained reducing conditions.63 Even though insensitive to conversion efficiency, and thus can serve as a this was exemplified for fossil crinoids in a pigment-rich Triassic robust tracer of soil-derived terrestrial organic matter. oil shale, these reactions likely also apply to the precursors of biogenic PAH. We deduce, therefore, that fungal-derived ■ ASSOCIATED CONTENT perylenequinone is deoxygenated during sediment diagenesis *S Supporting Information and, at least partly, survives coalification. This could explain the The Supporting Information is available free of charge on the occurrence of perylene in fossil deposits32 and could explain its ACS Publications website at DOI: 10.1021/acs.est.9b02344. abundance in combustion residues. One evolutionary rationale Details on the preparative chromatographic isolation of for the occurrence of perylene in scletoria, the resting structures fi 64 PAHs for compound-speci cisotopeanalysis,the of C. geophyllum, is the extreme mutagenic activity of the concept of two modes of terrigenous organic matter unsaturated nucleus of perylenequinones on Gram-negative 33 export from land to oceans, the impact of the nuclear bacteria, protecting the reproductive function of fungal spores. 14 17,22,32 weapon testing on the atmospheric and marine C Overall, the preponderance of evidence, reinforced by our partitioning over time and results for grain size analyses, new data, indicates that perylene is a remnant of wood respectively (PDF) degradation or fungal activity in the rhizosphere, a hotspot of biological activity on land, and source of organic matter to aquatic systems. ■ AUTHOR INFORMATION Parallels between Perylene and TOC. Sedimentary Corresponding Author organic matter is a highly complex mixture composed of aquatic *E-mail: [email protected]. and terrigenous organic carbon, and this complexity complicates ORCID source apportionment calculations, as well as determination of Ulrich M. Hanke: 0000-0002-4270-225X carbon fluxes and thus the carbon burial efficiencies.65,66 Christopher M. Reddy: 0000-0002-7814-2071 Measurement of the abundance and isotopic composition of fi Present Addresses source-speci c molecular markers can provide constraints on ∥ terrigenous organic matter in sediments.65 In addition to source (A.L.L.B.) ExxonMobil Exploration Company, Spring, Texas, 13 14 United States. constraints from δ C and C signatures, the latter also yields ⊥ information on whether organic matter is of modern or fossil (P.P.) Princeton University, 36 University Place, Princeton, origin,44 as well as on time scales of terrigenous organic matter New Jersey 08544, United States. between formation on land and burial in aquatic depocenters Notes (i.e., “average residence times”).35 The process of “pre-aging” The authors declare no competing financial interest. implies a time lag between biosynthesis and export of organic matter from land to depocenter, with natural as well as ■ ACKNOWLEDGMENTS anthropogenic molecules being retained in catchment soils We thank John King, Sean Sylva, Brad Hubeny, Peter Sauer, and 35,55,56 from annual to millennial time-scales. Here, we find that Jim Broda for their help in sampling; Carl Johnson and Daniel this pre-aging process occurs on similar time-scales for leaf wax Montlucoņ for their incessant help with analyses; as well as Mark fatty acids (n-alkanoic acids), biomass-derived pyrogenic carbon Yunker for critical discussion on the perils of perylene. Professor and the rhizosphere tracer perylene−all together terrestrial Phil Meyers and two anonymous reviewers provided comments markers with different modes of formation, chemical structures that improved the quality of the manuscript. U.M.H. acknowl- and functionalities. This agreement between these different edges the Swiss National Science Foundation for his source-specific markers suggests that retention within soils postdoctoral fellowship and T.I.E. and K.A.H. acknowledges regulates the export of most terrigenous organic matter and the NSF for research grants CHE-0089172 and OCE-9708478. associated carbon-based pollutants that enter the soil column. TOC and perylene MARs covary in the preindustrial era until ■ REFERENCES fl about 1850 despite some variability in the TOC ux (Figure 1). (1) Orr, W. L.; Grady, J. R. Perylene in Basin Sediments off Southern We attribute the latter to the increasing pressure by extensive California. Geochim. Cosmochim. 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